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OPINION published: 04 January 2017 doi: 10.3389/fpls.2016.01982

Conservation of Indigenous Vegetables from a Hotspot in Tropical Asia: What Did We Learn from Vavilov?

Svein Ø. Solberg * and Yu-Yu Chou

Theme Germplasm, World Vegetable Center, Tainan, Taiwan

Keywords: biodiversity, crop wild relative, geography, genetic resources, genebank, horticulture, vegetable

CROP DIVERSITY AND GEOGRAPHY

Conservation biologists have allocated an Indo-Burma biodiversity hotspot among 34 regions around the world especially rich in plants, animals, and other species (Myers et al., 2000). More than 13,500 different vascular plant species, of which 7000 are endemic, have been detected in this hotspot (Tordoff et al., 2012). Ninety years ago, the Russian scientist Vavilov (1926) pointed to the richness of cultivated plant species and their crop wild relatives in certain areas around the world, of which the Tropical Asia Center was one of eight. Later, Zeven and Zhukovsky (1975) applied the term Indochinese—Indonesian region of diversity for the area, which by then had Edited by: been divided by various authors into an Indochinese region including Myanmar, Laos, Cambodia, Paul Christiaan Struik, Thailand, Bangladesh, and parts of Northeastern India and Southern China, and a more southern Wageningen University and Research region including Malaysia and Indonesia (Darlington, 1956; Li, 1969; Schery, 1972; Janick, 2002; Centre, Netherlands Nandwani, 2014). Rice (Oryza sp.), mungbean (Vigna radiata), gourd species, and indigenous Reviewed by: vegetables were among crops that Zeven and Zhukovsky (1975) listed in the Indochinese region Samuel Rezende Paiva, of diversity. EMBRAPA Labex US—Secretariat of Vavilov noted the importance of collecting different varieties, and the wild relatives, of cultivated International Affairs, Brazil Robert Henry, plants as genetic resources for use in crop improvement. In 1935, he claimed that for plant breeders University of Queensland, Australia there was no other choice but to become geographers (Vavilov, 1935). At that time, the genepool *Correspondence: available to plant breeders was relatively narrow. To adapt crops to a wider geographical zone Svein Ø. Solberg and to move forward in breeding, Vavilov started collecting germplasm worldwide and conducted [email protected] expeditions to India, China, and other locations. He also received samples of leguminous species from Myanmar. In a later overseas collection mission in Myanmar, Kobylyanskaya, and Chepurin Specialty section: from the Vavilov Institute collected 201 accessions of cereals and legumes from the central and This article was submitted to south parts of the country (Loskutov, 1999). More recently, Japanese scientists have conducted Crop Science and Horticulture, missions to Myanmar to collect wild rice (Uga et al., 2004). a section of the journal As global populations increase and climates change, a greater diversity of genetic resources is Frontiers in Plant Science needed for crop improvement. Agriculture needs to produce more food under more unpredictable Received: 04 August 2016 climatic conditions (McCouch et al., 2013; Nierenberg, 2013; Betts and Hawkins, 2014). Genetic Accepted: 13 December 2016 resources have indeed been collected; according to the UN Food and Agriculture Organization Published: 04 January 2017 (FAO, 2010), rice is well-represented, with more than 770,000 accessions in genebanks around Citation: the world. Horticultural crops such as vegetables tend to be highly underrepresented in the Solberg SØ and Chou Y-Y (2017) conservation system, especially considering their nutritional importance (Yang and Hanson, 2009). Conservation of Indigenous Vegetables from a Hotspot in Tropical Here we demonstrate, despite 90 years of awareness, how indigenous vegetables are poorly Asia: What Did We Learn from represented in the global conservation system and argue for the importance of safeguarding Vavilov? Front. Plant Sci. 7:1982. agrobiodiversity in its centers of diversity. We use tropical Asia as a case area but narrow our focus doi: 10.3389/fpls.2016.01982 to Myanmar and indigenous vegetables relevant for this country.

Frontiers in Plant Science | www.frontiersin.org 1 January 2017 | Volume 7 | Article 1982 Solberg and Chou Conservation of Tropical Vegetables

MYANMAR AND TARGET CROPS SPECIES OCCURRENCES

Myanmar is within a recognized region of diversity of several In GBIF (2016), a total of 108,787 occurrences from Myanmar cultivated plants. The country has a tropical monsoon climate, were reported, which was <0.02% out of the global number of a distinct wet and warm summer and a dry and relatively 645,184,811. Of targeted species, there were the most records warm winter. The current population is 51.7 million. Myanmar from Myanmar on Senegalia pennata (climbing wattle), a wild is a member of the Association of Southeast Asian Nations tree not mentioned by Zeven and Zhukovsky (1975), its leaves (ASEAN) and recently joined the ASEAN economic community. are collected and used as a vegetable, followed by Cajanus cajan Agriculture is important and generates more than 20% of export (pigeon pea), a grain legume not included in the Indochina region earnings and employs more than 60% of the labor force (MOAI, of diversity (Table 1). Of the species with Indochina as the region 2015). Rice is cultivated on two thirds of the arable land; around of diversity, Trichosanthes cucumerina (snake gourd), Momordica 1 million tons of rice are exported annually. Pulses are the charantia (bitter gourd), and Vigna radiata (mungbean) each second most important crop, grown on 4.5 million ha, and had four to seven records from Myanmar in GBIF, which include species such as black gram and mungbean (green gram). were herbarium specimens or seed collects. These are very low Vegetables are grown on around 0.8 million ha, principally numbers, but they do not necessarily reflect the importance or the in the highlands but also in household gardens or small- presence of the species. Rather, this can be a result of few botanic scale market gardens throughout the country. The conservation studies or no reporting from the country to GBIF. system of plant genetic resources in Myanmar is organized by the Department of Agricultural Research with national seed and field CONSERVATION STATUS collections and a common information system maintained at the Myanmar Seed Bank and funded by the government of Japan In GENESYS (2016), a total number of 4092 accessions with (FAO, 2016). Myanmar as country of origin were reported, which was We were interested in vegetable crops that Zeven and 0.16% out of the global number of 2,573,870 accessions. Zhukovsky (1975) linked to Tropical Asia and Myanmar as Targeted vegetable species had from 0 to 20,000 conserved region of diversity. They used the term “S. Asia” for this area accessions globally, but only with 0–70 accessions from Myanmar in contrast to SE. Asia, which was used for the more southern depending on the species (Table 1). Mungbean was relatively area including Malaysia and Indonesia. Typical medicinal plants, well-represented in genebanks around the world, but had only bamboo species, and starch plants were not included, although a very few accessions from Myanmar; a country mentioned some would call them vegetables. In addition, a second list as the primary region of diversity by Zeven and Zhukovsky of vegetable crops was made based on those regarded as (1975). In contrast, India is represented by 5154 mungbean important indigenous vegetables in Myanmar today by national accessions in GENESYS. The overall underrepresentation of agricultural experts from the Seed Bank Myanmar, Department indigenous vegetables from Tropical Asia is clear. In total, 451 of Agricultural Research, or as presented in a publication of accessions of bitter gourd were reported in GENESYS, none important food plants in Myanmar (Watanbe et al., 1999). The with Myanmar as country of origin, and 81 accessions of the two lists were merged and more than 30 target species were leafy vegetable kangkong (Ipomoea aquatica) were reported, also identified (Table 1). with none from Myanmar. As a comparison, rice (Oryza sp.) The Integrated Taxonomic Information System was applied has 208,447 accessions in GENESYS (and 3543 accessions with (ITIS, 2016) to verify the species taxonomic and common Myanmar as country of origin). Among the reported bitter gourd names. Each species was then examined by surveying two accessions 50 were from Thailand, 40 from Bangladesh, 32 from global databases: the Global Biodiversity Information Facility Cambodia, and 0 from Myanmar—all countries regarded as (GBIF, 2016) and the Global Gateway to Genetic Resources part of the primary region of diversity. Among the kangkong (GENESYS, 2016). GBIF was applied to survey the number accessions 27 were from Thailand, 4 from Cambodia and again, of occurrences, applying the scientific names and country 0 from Myanmar. These numbers are all very low. Both bitter filters in the search function. GBIF (2016) occurrences are gourd and kangkong are common in smallholder gardens in the recorded number of observations of a species as natural Myanmar and other tropical Asian countries. The crops may populations, herbarium specimens, seed collects, or others. likely be present as semi-wild, naturalized populations, as locally GENESYS (2016) records reflect the conservation status of cultivated material (landraces), or as modern varieties. GENESYS plant genetic resources. GENESYS was applied to survey the does not capture all conserved germplasm, as there are collection number of conserved accessions, applying the scientific names holders that do not report to the global database. However, and country of origin as filters in the search function. In surveying the database gives a guideline of the conservation GENESYS, combined searches were used; for example for status. A crop such as bitter gourd is used all over tropical mungbean, different taxa, and authors were combined including Asia, the plant is related to cucumber, and it has several Vigna radiata var. radiate, Vigna radiata (L.) R. Wilczek var. positive health effects, including being good for lowering blood radiate, Vigna radiate, Vigna radiata (L.) R. Wilczek var. sugar levels (Leung et al., 2009). Kangkong is a nutritious radiate, Vigna radiata (L.) R. wilczek, and Vigna radiata (L.) leafy vegetable that can stand wet conditions and flooding R.Wilczek. Filters used are given as Supplementary Material (Irfanullah et al., 2011), and thus has potential for climate change (Table S1). adaptation.

Frontiers in Plant Science | www.frontiersin.org 2 January 2017 | Volume 7 | Article 1982 Solberg and Chou Conservation of Tropical Vegetables

TABLE 1 | Targeted species, their region of diversity, number of occurrences, and number of conserved accessions globally and with Myanmar as country of origin.

Scientific and common name Region of No. of occurrences No. of accessions diversityA GBIF (2016) GENESYS (2016)

Global Myanmar Global Myanmar

VEGETABLE SPECIES WITH DIVERSITY CENTER INCLUDING MYANMAR Vigna radiata (mungbean) India, Myanmar 11,879 4 11,953 10 Wolffia arrhiza (spotless watermeal) India, Myanmar 10,223 0 0 0 Momordica charantia (bittergourd) TAsia 6044 5 451 0 Ocimum basilicum (sweetbasil) TAsia 3083 0 444 0 Oenanthe javanica (Chinese celery) Indochina 3066 2 3 0 Mucuna pruriens (Cochichina) T Asia 2220 6 48 0 Vigna mungo (black gram) India, Myanmar 1929 2 1518 0 Luffa aegyptiaca (spongegourd) India,TAsia 1583 4 532 1 Amaranthus tricolor (amaranth) T Asia 1248 0 473 0 Basella alba (Indian spinach) T Asia 1051 5 170 0 Trichosanthes cucumerina (snakegourd) TAsia 963 7 46 0 Neptunia oleracea (gardenpuff) TAsia 937 2 9 0 Psophocarpus tetragonolobus (winged bean) T Asia 839 1 485 0 Benincasa hispida (waxgourd) TAsia 513 1 383 0 Canavalia gladiata (sword jackbean) Myanmar 349 3 28 0 Sesbania grandiflora (veg. hummingbird) T Asia 6 0 114 0 INDIGENOUS VEGETABLES IMPORTANT FOR MYANMARB BUT FROM OTHER DIVERSITY CENTERS Vigna unguiculata (cowpea) Africa, India 37,203 2 19,429 4 Brassica nigra (black mustard) Europe 19,824 0 231 0 Cajanus cajan (pigeon pea) Africa, India 17,439 14 13,590 74 Sinapis alba (white mustard) Europe 14,471 0 538 0 Phaseolus lunatus (Lima bean) C America 9268 1 6088 2 Solanum melongena (eggplant) India, China 5831 7 5487 6 Hibiscus cannabinus (roselle) Africa 5370 3 553 0 Lagenaria siceraria (bottlegourd) Africa 2551 1 1172 1 Colocasia esculenta (wild taro) SE Asia 2266 1 0 0 Ipomoea aquatica (kangkong) Noinfo 1977 7 81 0 Pachyrhizus erosus (ice potato) S America 1310 0 83 0 Nelumbo nucifera (lotus) CAsia 1060 3 2 0 Sechium edule (chayote) C America 900 0 6 0 Artocarpus heterophyllus (jackfruit) India 868 0 15 0 Luffa acutangula (spongegourd) India 759 3 551 0 Senegalia pennata (climbing wattle) 685 18 0 0 Amorphophallus paeoniifolius (elephant yam) SE Asia 570 1 3 0 Dolichos lablab (lablab bean) Africa 565 0 16 0 Centella erecta (Asian pennywort) No info 297 0 0 0 Combretum indicum (Rangoon creeper) SE Asia 260 0 1 0 Lablab vulgaris (summer bean) No info 53 0 0 0

A grand total number of occurrences in GBIF (2016) was 645,184,811 with 108,787 from Myanmar. A grand total number of conserved accessions in GENESYS (2016) was 2,573,870 with 4092 accessions with Myanmar as country of origin. ACenter of diversity according to Zeven and Zhukovsky (1975) (T Asia, Triopical Asia), BImportant vegetables in Myanmar according to Watanbe et al. (1999) and national agricultural expertise.

OUTLOOK are being introduced (Asian Development Bank Institute, 2013; MOAI, 2016). Ongoing changes imply that important plant Myanmar is experiencing significant economic and political genetic resources in a recognized region of diversity may be changes (Asian Development Bank, 2012). Its agricultural sector threatened. We have demonstrated that today such genetic is evolving; seed companies are establishing; and new cultivars resources are sparsely represented in global collections. As

Frontiers in Plant Science | www.frontiersin.org 3 January 2017 | Volume 7 | Article 1982 Solberg and Chou Conservation of Tropical Vegetables gaps have been identified, new collection missions should complicating the access of enterprises and research institutions be conducted. This should be done to safeguard the genetic to genetic material. To paraphrase Vavilov: Plant breeders are resources and also to facilitate access for breeding and research restricted from being geographers. Such constraints hinder the as outlined in the International Treaty on Plant Genetic Resources best efforts of agriculture to face the grand challenges of our time. for Food and Agriculture (ITPGRFA, 2001). One problem is that International organizations, national policy makers, research most vegetables, and almost all indigenous vegetables, are not institutions, and enterprises should work together and find joint explicitly mentioned in Annex 1 of the Treaty. Furthermore, solutions to safeguard and utilize the great potential of plant the Convention of Biological Diversity and the Nagoya Protocol genetic resources. on Access and Benefit Sharing (ABS, 2014) has made overseas collection missions complicated (Cressey, 2014; Maggioni et al., AUTHOR CONTRIBUTIONS 2015). Ninety yeas after Vavilov published his work on Centers of Origin, there are still huge gaps in global collections. Although SS had the idea and contributed by co-ordination the writing. YC some major crops have been extensively collected, indigenous contributed by database searches and comments. vegetables from tropical Asia, and especially from Myanmar, are poorly represented. Such vegetables have great potential SUPPLEMENTARY MATERIAL to add vital nutrients to human diets (Yang and Hanson, 2009), diversify cropping systems (Subbarao et al., 2005), and The Supplementary Material for this article can be found increase smallholders’ incomes and livelihoods (Ebert, 2014). online at: http://journal.frontiersin.org/article/10.3389/fpls.2016. Indeed, there are challenges ahead: What Vavilov once did is 01982/full#supplementary-material difficult to do today. Now, each country tends to guard its Table S1 | Scientific names applied as filters in the search function in domain; some countries look more inwards than outwards, GENESYS.

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Vavilov, N. I. (1926). Studies on the origin of cultivated plants. (Russian) Bull. Appl. and Lower Plants. Wageningen: Centre for Agricultural Publishing and Bot. Plant Breeding 14, 1–245. Documentation. Vavilov, N. I. (1935). “Theoretical Basis for Plant Breeding,” in Origin and Geography of Cultivated Plants, Vol. 1, The Phytogeographical Basis for Plant Conflict of Interest Statement: The authors declare that the research was Breeding Moscow, Transl. by D. Love (Cambridge: Cambridge University conducted in the absence of any commercial or financial relationships that could Press), 316–366. be construed as a potential conflict of interest. Watanbe, S., Tananka, H., Ito, M., and Irie, K. (1999). Useful Plants in Myanmar. Nay Pyi Taw: Central Agricultural Research Institute. Copyright © 2017 Solberg and Chou. This is an open-access article distributed Yang, R. Y., and Hanson, P. (2009). Improved food availability for under the terms of the Creative Commons Attribution License (CC BY). The use, food security in Asia-Pacific region. Asia Pac. J. Clin. Nutr. 18, distribution or reproduction in other forums is permitted, provided the original 633–337 author(s) or licensor are credited and that the original publication in this journal Zeven, A. C., and Zhukovsky, P. M. (1975). Dictionary of Cultivated Plants is cited, in accordance with accepted academic practice. No use, distribution or and Their Centres of Diversity - Excluding Ornamentals, Forest Trees reproduction is permitted which does not comply with these terms.

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